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PDV2 has a dosage effect on chloroplast division in Arabidopsis

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PDV2 has a dosage effect on chloroplast division in Arabidopsis thaliana , but this effect may vary in different plants.

Abstract

Chloroplasts have to be divided as plants grow to maintain an optimized number in the cell. Chloroplasts are divided by protein complexes across the double membranes from the stroma side to the cytosolic side. PDV2 is a chloroplast division protein on the chloroplast outer membrane. It recruits the dynamin-related GTPase ARC5 to the division site. The C-terminus of PDV2 and the C-terminus of ARC6 interact in the intermembrane space, which is important for the localization of PDV2. Previously, it was shown that overexpression of PDV2 can increase the division of chloroplasts in Arabidopsis and moss, so the authors concluded that PDV2 determines the rate of chloroplast division in land plants. PDV2 was also shown to inhibit the GTPase activity of ARC5 by in vitro experiment. These results look to be contradictory. Here, we identified a null allele of PDV2 in Arabidopsis and studied plants with different levels of PDV2. Our results suggested that the chloroplast division phenotype in Arabidopsis is sensitive to the level of PDV2, while this is not the case for ARC6. The level of PDV2 protein is reduced sharply in fast-growing leaves, while the level of ARC6 is not. The levels of PDV2 and ARC6 in several other plant species at different developmental stages were also investigated. The results indicated that their expression pattern varies in different species. Thus, PDV2 is an important positive factor of chloroplast division with an apparent dosage effect in Arabidopsis, but this effect for different chloroplast division proteins in different plants may vary.

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References

  • Bates PD, Johnson SR, Cao X, Li J, Nam JW, Jaworski JG, Ohlrogge JB (2014) Fatty acid synthesis is inhibited by inefficient utilization of unusual fatty acids for glycerolipid assembly. Proc Natl Acad Sci USA 111:1204–1209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang N, Gao Y, Zhao L, Liu X, Gao H (2015) Arabidopsis FHY3/CPD45 regulates far-red light signaling and chloroplast division in parallel. Sci Rep 5:1–6

    Google Scholar 

  • Colletti KS, Tattersall EA, Pyke KA, Froelich JE, Stokes KD, Osteryoung KW (2000) A homologue of the bacterial cell division site-determining factor MinD mediates placement of the chloroplast division apparatus. Curr Biol 10:507–516

    Article  CAS  PubMed  Google Scholar 

  • Fujiwara MT, Hashimoto H, Kazama Y, Abe T, Yoshida S, Sato N, Itoh RD (2008) The assembly of the FtsZ ring at the mid-chloroplast division site depends on a balance between the activities of AtMinE1 and ARC11/AtMinD1. Plant Cell Physiol 49:345–361

    Article  CAS  PubMed  Google Scholar 

  • Gao H, Kadirjan-Kalbach D, Froehlich JE, Osteryoung KW (2003) ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery. PNAS 100:4328–4333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao Y, Liu H, An C, Shi Y, Liu X, Yuan W, Zhang B, Yang J, Yu C, Gao H (2013) Arabidopsis FRS4/CPD25 and FHY3/CPD45 work cooperatively to promote the expression of the chloroplast division gene ARC5 and chloroplast division. Plant J 75:795–807

    Article  CAS  PubMed  Google Scholar 

  • Glynn JM, Sy Miyagishima, Yoder DW, Osteryoung KW, Vitha S (2007) Chloroplast division. Traffic 8:451–461

    Article  CAS  PubMed  Google Scholar 

  • Glynn JM, Froehlich JE, Osteryoung KW (2008) Arabidopsis ARC6 coordinates the division machineries of the inner and outer chloroplast membranes through interaction with PDV2 in the intermembrane space. Plant Cell 20:2460–2470

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glynn JM, Yang Y, Vitha S, Schmitz AJ, Hemmes M, Sy Miyagishima, Osteryoung KW (2009) PARC6, a novel chloroplast division factor, influences FtsZ assembly and is required for recruitment of PDV1 during chloroplast division in Arabidopsis. Plant J 59:700–711

    Article  CAS  PubMed  Google Scholar 

  • Holtsmark I, Lee S, Lunde KA, Auestad K, Maple-Grødem J, Møller SG (2013) Plastid division control: the PDV proteins regulate DRP5B dynamin activity. Plant Mol Biol 82:255–266

    Article  CAS  PubMed  Google Scholar 

  • Itoh R, Fujiwara M, Nagata N, Yoshida S (2001) A chloroplast protein homologous to the eubacterial topological specificity factor MinE plays a role in chloroplast division. Plant Physiol 127:1644–1655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson CB, Tang LK, Smith AG, Ravichandran A, Luo Z, Vitha S, Holzenburg A (2013) Single particle tracking analysis of the chloroplast division protein FtsZ anchoring to the inner envelope membrane. Microsc Microanal 19:507–512

    Article  CAS  PubMed  Google Scholar 

  • Kuroiwa T, Kuroiwa H, Sakai A, Takahashi H, Toda K, Itoh R (1998) The division apparatus of plastids and mitochondria. Int Rev Cytol 181:1–41

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Sun Q, Feng Y, Liu X, Gao H (2016) An improved immunofluorescence staining method for chloroplast proteins. Plant Cell Rep 35:2285–2293

    Article  CAS  PubMed  Google Scholar 

  • Maple J, Vojta L, Soll J, Møller SG (2007) ARC3 is a stromal Z-ring accessory protein essential for plastid division. EMBO Rep 8:293–299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McFadden GI (2001) Chloroplast origin and integration. Plant Physiol 125:50–53

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noctor G, Arisi A-CM, Jouanin L, Foyer CH (1998) Manipulation of glutathione and amino acid biosynthesis in the chloroplast. Plant Physiol 118:471–482

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okazaki K, Kabeya Y, Suzuki K, Mori T, Ichikawa T, Matsui M, Nakanishi H, S-y Miyagishima (2009) The PLASTID DIVISION1 and 2 components of the chloroplast division machinery determine the rate of chloroplast division in land plant cell differentiation. Plant Cell 21:1769–1780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Olson BJ, Wang Q, Osteryoung KW (2010) GTP-dependent heteropolymer formation and bundling of chloroplast FtsZ1 and FtsZ2. J Biol Chem 285:20634–20643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osteryoung KW, Pyke KA (2014) Division and dynamic morphology of plastids. Annu Rev Plant Biol 65:443–472

    Article  CAS  PubMed  Google Scholar 

  • Pyke KA, Rutherford SM, Robertson EJ, Leech RM (1994) arc6, a fertile Arabidopsis mutant with only two mesophyll cell chloroplasts. Plant Physiol 106:1169–1177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seay M, Hayward AP, Tsao J, Dinesh-Kumar S (2009) Something old, something new: plant innate immunity and autophagy. Autophagy in infection and immunity. Springer, Berlin, Heidelberg, pp 287–306

    Chapter  Google Scholar 

  • Miyagishima SY, Froehlich JE, Osteryoung KW (2006) PDV1 and PDV2 mediate recruitment of the dynamin-related protein ARC5 to the plastid division site. Plant Cell 18:2517–2530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tveitaskog AE, Maple J, Møller SG (2007) Plastid division in an evolutionary context. Biol Chem 388:937–942

    Article  CAS  PubMed  Google Scholar 

  • Vitha S, McAndrew RS, Osteryoung KW (2001) FtsZ ring formation at the chloroplast division site in plants. J Cell Biol 153:111–120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vitha S, Froehlich JE, Koksharova O, Pyke KA, van Erp H, Osteryoung KW (2003) ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell 15:1918–1933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida Y, SY Miyagishima, Kuroiwa H, Kuroiwa T (2012) The plastid-dividing machinery: formation, constriction and fission. Curr Opin Plant Biol 15:714–721

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, Jia N, Li H, Gao H-B (2015) Identification and analysis of ARC6 gene in a chloroplast division mutant cpd44 in Arabidopsis thaliana. Plant Physiol J 51:501–508

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the National Natural Science Foundation of China (31070162, 31501090, and 31400635).

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Correspondence to Xiaomin Liu.

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The authors claim no competing interests.

Additional information

Communicated by Q. Zhao.

N. Chang and Q. Sun contributed equally to this work.

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Chang, N., Sun, Q., Li, Y. et al. PDV2 has a dosage effect on chloroplast division in Arabidopsis . Plant Cell Rep 36, 471–480 (2017). https://doi.org/10.1007/s00299-016-2096-6

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  • DOI: https://doi.org/10.1007/s00299-016-2096-6

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